Community structure of insect herbivores is driven by conservatism, escalation and divergence of defensive traits in Ficus

Martin Volf; Simon T. Segar; Scott E. Miller; Brus Isua; Mentap Sisol; Gibson Aubona; Petr Šimek; Martin Moos; Juuso Laitila; Jorma Kim; Jan Zima; Jadranka Rota; George D. Weiblen; Stewart Wossa; Juha Pekka Salminen; Yves Basset; Vojtech Novotny

doi:10.1111/ele.12875

Community structure of insect herbivores is driven by conservatism, escalation and divergence of defensive traits in Ficus

Martin Volf, Simon T. Segar, Scott E. Miller, Brus Isua, Mentap Sisol, Gibson Aubona, Petr Šimek, Martin Moos, Juuso Laitila, Jorma Kim, Jan Zima, Jadranka Rota, George D. Weiblen, Stewart Wossa, Juha Pekka Salminen, Yves Basset, Vojtech Novotny

Plant and Microbial Biology

Research output: Contribution to journal › Letter › peer-review

60 Scopus citations

Abstract

Escalation (macroevolutionary increase) or divergence (disparity between relatives) in trait values are two frequent outcomes of the plant-herbivore arms race. We studied the defences and caterpillars associated with 21 sympatric New Guinean figs. Herbivore generalists were concentrated on hosts with low protease and oxidative activity. The distribution of specialists correlated with phylogeny, protease and trichomes. Additionally, highly specialised Asota moths used alkaloid rich plants. The evolution of proteases was conserved, alkaloid diversity has escalated across the studied species, oxidative activity has escalated within one clade, and trichomes have diverged across the phylogeny. Herbivore specificity correlated with their response to host defences: escalating traits largely affected generalists and divergent traits specialists; but the effect of escalating traits on extreme specialists was positive. In turn, the evolution of defences in Ficus can be driven towards both escalation and divergence in individual traits, in combination providing protection against a broad spectrum of herbivores.

Original language	English (US)
Pages (from-to)	83-92
Number of pages	10
Journal	Ecology letters
Volume	21
Issue number	1
DOIs	https://doi.org/10.1111/ele.12875
State	Published - Jan 2018

Bibliographical note

Funding Information:
We thank the staff of the New Guinea Binatang Research Centre in Papua New Guinea. STS acknowledges funding from a USB Postdoc project reg.no. CZ.1.07/2.3.00/30.0006 (funded by the European Social Fund and the Czech State Budget) and Grant Agency of the Czech Republic 15-24571S. MV acknowledges funding from the Grant Agency of the University of South Bohemia GAJU 156/2013/P and GAJU 103-016/2015/P. VN acknowledges the European Science Foundation grant 669609, Darwin Initiative project no. 22-002, and Grant Agency of the Czech Republic 17-23862S. We acknowledge US National Science Foundation DEB 9407297. JPS acknowledges funding from the Academy of Finland (grant no 258992), and the help of Saku Valkamaa, Atte Tuominen and Anne Koivuniemi in the chemical analyses. We thank the Papua New Guinea Forest Research Institute, in particular Kipiro Damas, for assistance granting export permits. We also thank again those acknowledged in Novotny et al. (2010), especially colleagues at the Natural History Museum, London, for taxonomic assistance. We thank Petr Klimesˇ and Philip T. Butterill for constructive criticism of the manuscript and Will Pearse and Petr Sˇ milauer for analytical advice. Access to computing and storage facilities owned by parties and projects contributing to the National Grid Infrastructure MetaCentrum provided under the programme ‘Projects of Large Research, Development, and Innovations Infrastructures’ (CESNET LM2015042), is greatly appreciated. In addition, we thank the editors and anonymous reviewers for their valuable comments, which greatly improved the manuscript.

Publisher Copyright:
© 2017 John Wiley & Sons Ltd/CNRS

Keywords

Alkaloids
Choreutidae
Lepidoptera
New Guinea
Pyraloidea
coevolution
cysteine protease
herbivore
polyphenols
trichomes

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

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Volf, M., Segar, S. T., Miller, S. E., Isua, B., Sisol, M., Aubona, G., Šimek, P., Moos, M., Laitila, J., Kim, J., Zima, J., Rota, J., Weiblen, G. D., Wossa, S., Salminen, J. P., Basset, Y., & Novotny, V. (2018). Community structure of insect herbivores is driven by conservatism, escalation and divergence of defensive traits in Ficus. Ecology letters, 21(1), 83-92. https://doi.org/10.1111/ele.12875

Volf, M, Segar, ST, Miller, SE, Isua, B, Sisol, M, Aubona, G, Šimek, P, Moos, M, Laitila, J, Kim, J, Zima, J, Rota, J, Weiblen, GD, Wossa, S, Salminen, JP, Basset, Y & Novotny, V 2018, 'Community structure of insect herbivores is driven by conservatism, escalation and divergence of defensive traits in Ficus', Ecology letters, vol. 21, no. 1, pp. 83-92. https://doi.org/10.1111/ele.12875

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title = "Community structure of insect herbivores is driven by conservatism, escalation and divergence of defensive traits in Ficus",

abstract = "Escalation (macroevolutionary increase) or divergence (disparity between relatives) in trait values are two frequent outcomes of the plant-herbivore arms race. We studied the defences and caterpillars associated with 21 sympatric New Guinean figs. Herbivore generalists were concentrated on hosts with low protease and oxidative activity. The distribution of specialists correlated with phylogeny, protease and trichomes. Additionally, highly specialised Asota moths used alkaloid rich plants. The evolution of proteases was conserved, alkaloid diversity has escalated across the studied species, oxidative activity has escalated within one clade, and trichomes have diverged across the phylogeny. Herbivore specificity correlated with their response to host defences: escalating traits largely affected generalists and divergent traits specialists; but the effect of escalating traits on extreme specialists was positive. In turn, the evolution of defences in Ficus can be driven towards both escalation and divergence in individual traits, in combination providing protection against a broad spectrum of herbivores.",

keywords = "Alkaloids, Choreutidae, Lepidoptera, New Guinea, Pyraloidea, coevolution, cysteine protease, herbivore, polyphenols, trichomes",

author = "Martin Volf and Segar, {Simon T.} and Miller, {Scott E.} and Brus Isua and Mentap Sisol and Gibson Aubona and Petr {\v S}imek and Martin Moos and Juuso Laitila and Jorma Kim and Jan Zima and Jadranka Rota and Weiblen, {George D.} and Stewart Wossa and Salminen, {Juha Pekka} and Yves Basset and Vojtech Novotny",

note = "Funding Information: We thank the staff of the New Guinea Binatang Research Centre in Papua New Guinea. STS acknowledges funding from a USB Postdoc project reg.no. CZ.1.07/2.3.00/30.0006 (funded by the European Social Fund and the Czech State Budget) and Grant Agency of the Czech Republic 15-24571S. MV acknowledges funding from the Grant Agency of the University of South Bohemia GAJU 156/2013/P and GAJU 103-016/2015/P. VN acknowledges the European Science Foundation grant 669609, Darwin Initiative project no. 22-002, and Grant Agency of the Czech Republic 17-23862S. We acknowledge US National Science Foundation DEB 9407297. JPS acknowledges funding from the Academy of Finland (grant no 258992), and the help of Saku Valkamaa, Atte Tuominen and Anne Koivuniemi in the chemical analyses. We thank the Papua New Guinea Forest Research Institute, in particular Kipiro Damas, for assistance granting export permits. We also thank again those acknowledged in Novotny et al. (2010), especially colleagues at the Natural History Museum, London, for taxonomic assistance. We thank Petr Klimesˇ and Philip T. Butterill for constructive criticism of the manuscript and Will Pearse and Petr Sˇ milauer for analytical advice. Access to computing and storage facilities owned by parties and projects contributing to the National Grid Infrastructure MetaCentrum provided under the programme {\textquoteleft}Projects of Large Research, Development, and Innovations Infrastructures{\textquoteright} (CESNET LM2015042), is greatly appreciated. In addition, we thank the editors and anonymous reviewers for their valuable comments, which greatly improved the manuscript. Publisher Copyright: {\textcopyright} 2017 John Wiley & Sons Ltd/CNRS",

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AU - Volf, Martin

AU - Segar, Simon T.

AU - Miller, Scott E.

AU - Isua, Brus

AU - Sisol, Mentap

AU - Aubona, Gibson

AU - Šimek, Petr

AU - Moos, Martin

AU - Laitila, Juuso

AU - Kim, Jorma

AU - Zima, Jan

AU - Rota, Jadranka

AU - Weiblen, George D.

AU - Wossa, Stewart

AU - Salminen, Juha Pekka

AU - Basset, Yves

AU - Novotny, Vojtech

N1 - Funding Information: We thank the staff of the New Guinea Binatang Research Centre in Papua New Guinea. STS acknowledges funding from a USB Postdoc project reg.no. CZ.1.07/2.3.00/30.0006 (funded by the European Social Fund and the Czech State Budget) and Grant Agency of the Czech Republic 15-24571S. MV acknowledges funding from the Grant Agency of the University of South Bohemia GAJU 156/2013/P and GAJU 103-016/2015/P. VN acknowledges the European Science Foundation grant 669609, Darwin Initiative project no. 22-002, and Grant Agency of the Czech Republic 17-23862S. We acknowledge US National Science Foundation DEB 9407297. JPS acknowledges funding from the Academy of Finland (grant no 258992), and the help of Saku Valkamaa, Atte Tuominen and Anne Koivuniemi in the chemical analyses. We thank the Papua New Guinea Forest Research Institute, in particular Kipiro Damas, for assistance granting export permits. We also thank again those acknowledged in Novotny et al. (2010), especially colleagues at the Natural History Museum, London, for taxonomic assistance. We thank Petr Klimesˇ and Philip T. Butterill for constructive criticism of the manuscript and Will Pearse and Petr Sˇ milauer for analytical advice. Access to computing and storage facilities owned by parties and projects contributing to the National Grid Infrastructure MetaCentrum provided under the programme ‘Projects of Large Research, Development, and Innovations Infrastructures’ (CESNET LM2015042), is greatly appreciated. In addition, we thank the editors and anonymous reviewers for their valuable comments, which greatly improved the manuscript. Publisher Copyright: © 2017 John Wiley & Sons Ltd/CNRS

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N2 - Escalation (macroevolutionary increase) or divergence (disparity between relatives) in trait values are two frequent outcomes of the plant-herbivore arms race. We studied the defences and caterpillars associated with 21 sympatric New Guinean figs. Herbivore generalists were concentrated on hosts with low protease and oxidative activity. The distribution of specialists correlated with phylogeny, protease and trichomes. Additionally, highly specialised Asota moths used alkaloid rich plants. The evolution of proteases was conserved, alkaloid diversity has escalated across the studied species, oxidative activity has escalated within one clade, and trichomes have diverged across the phylogeny. Herbivore specificity correlated with their response to host defences: escalating traits largely affected generalists and divergent traits specialists; but the effect of escalating traits on extreme specialists was positive. In turn, the evolution of defences in Ficus can be driven towards both escalation and divergence in individual traits, in combination providing protection against a broad spectrum of herbivores.

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KW - New Guinea

KW - Pyraloidea

KW - coevolution

KW - cysteine protease

KW - herbivore

KW - polyphenols

KW - trichomes

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ER -

Community structure of insect herbivores is driven by conservatism, escalation and divergence of defensive traits in Ficus

Abstract

Bibliographical note

Keywords

UN SDGs

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